Source: UNIV OF WISCONSIN submitted to NRP
HARNESSING IRON METABOLISM TO LIMIT SALMONELLA IN PRE- AND POST-HARVEST POULTRY
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1030478
Grant No.
2023-67017-40057
Cumulative Award Amt.
$297,000.00
Proposal No.
2022-09024
Multistate No.
(N/A)
Project Start Date
May 1, 2023
Project End Date
Apr 30, 2026
Grant Year
2023
Program Code
[A1332]- Food Safety and Defense
Recipient Organization
UNIV OF WISCONSIN
21 N PARK ST STE 6401
MADISON,WI 53715-1218
Performing Department
(N/A)
Non Technical Summary
This project will test the efficacy of promising new bioenergetic solutions to improve animal health and limit the transmission of harmful bacterial pathogens.
Animal Health Component
50%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
72232991170100%
Goals / Objectives
The goal of this proposal is to test a new method for controlling food-born bacterial infections: encapsulate iron. Specifically, we will determine how encapsulated iron affects S. enterica growth, virulence, and competitive interactions with beneficial gut microbes using established in vitro cecal and intestinal models and next-generation sequencing methods. We will also evaluate the anti-Salmonella therapeutic efficacy of SQM on infected broiler chickens by tracking the growth and gene expression of S. enterica during key pre- and post-harvest stages.These studies will provide critical information for how functional feed supplements might be used as a weapon against S. enterica. More broadly, given the conserved nature of iron metabolism across bacteria, we expect these data and methods will carry applications for other pathogens beyond S. enterica and carry much-needed non-pharmacological solutions to combating antimicrobial resistance.
Project Methods
Our long-term objective is to develop, empirically parameterize, and refine a multi-scale modeling framework that integrates across the molecular, organismal, and population levels.This project will contribute practical solutions for improving food safety and security and reducing pathogen spillovers from livestock to humans and the environment. Poultry studies focused on iron-Salmonella interactions remain particularly limited.While studies in poultry eggs demonstrate the important role that iron plays in Salmonella dynamics, most of our understanding of iron and Salmonella pathogenesis comes from rodent and mammalian cell culture assays, but conclusions drawn from these studies may not effectively translate to avian systems due to key physiological and morphological differences that affect how pathogens interact with avian environments. Thus, new animal models are needed to fill gaps left by mammalian Salmonella models. Our project will address these gaps in knowledge by integrating molecular, organismal, and population-level processes to provide key information on critical, but overlooked, aspects of Salmonella establishment, growth, virulence, and transmission. Together, these data will allow us to make recommendations on feed modifications and their effects on Salmonella and poultry health, including the gut microbiome, which would substantially reduce pre-harvest Salmonella and serve as practical diagnostic tools.Aim 1: Determine how iron availability affects within-host processes. Using established in vitro models, we will test the net effects of iron availability through multiple, potentially conflicting pathways. We hypothesize the encapsulated iron reduces metabolic syndrome, inflammation, and 'leaky gut' syndrome in the host, support beneficial gut microbes to enable competitive exclusion of S. enterica, but could increase the expression of virulence factors which pathogens use to acquire iron.Our preliminary aerobic in vitro data demonstrate that encapsulated limits the growth of S. enterica. These results provide proof of concept that encapsulated iron differentially reduces S. enterica growth relative to standard iron sources in commercial poultry feed (e.g., iron sulfate). However, it is unclear whether these in vitro results will hold in the anaerobic avian gut, and when S. enterica is in competition with gut microbes. For example, if gut microbes are more sensitive to iron limitation than S. enterica, then the in vitro pattern could reverse due to encapsulated iron limiting competition. We will build on these results to obtain a more integrated view of how iron affects the establishment and maintenance of S. enterica in avian environments. We have developed a novel in vitro poultry intestine-cecal model conducted in an anaerobic Coy Glove Box. Based on our previously published methods, this in vitro model allows us to determine encapsulated iron's impact on Salmonella growth and virulence in the presence of intestinal and cecal microbiota -- without the complex interactions of the host immune system.With this assay, we can track multiple variables simultaneously, reduce costs and time constraints by using a limited number of animals: ceca and intestines are collected from abattoirs, reducing the live animals required by 90%. Additionally, we can collect time-series data of these within-host interactions without causing undue stress to live animals. Thus, this in vitro model allows us to track key processes in the life cycle of Salmonella pathogenesis under different dietary conditions while reducing the logistical and welfare concerns of tracking infections in live birds. Using our established in vitro models combined with RT-PCR and Salmonella whole genome sequencing, we will test a series of interrelated hypotheses:Aim 1 H1: Encapsulated iron supports beneficial gut microbes that can outcompete S. enterica.Aim 1 H2: Encapsulated reduces excess free iron available to S. enterica.Aim 1 H3: Encapsulated iron reduces S. enterica growth rates and load.Aim 1 H4: Encapsulated iron reduces the expression of energetically costly traits that confer drug resistance (e.g., efflux pumps, plasmid acquisition).Aim 1 H5: Encapsulated iron increases expression of virulence factors that enable the pathogen to steal iron from the host and maintain iron homeostasis.Together, the relative influence of factors in H1-H5 (along with gut inflammation and permeability) will govern epidemiological and evolutionary effects of iron on S. enterica (future directions).Together, data from Aim 1 will provide key insight into the effects of iron on S. enterica via multiple, potentially interrelated pathways that operate at the molecular and cellular levels. The resulting time-series data on within-host processes are critical to developing and parameterizing multi-scale epidemiological and evolutionary models (future directions).All results will be analyzed using generalized linear models and generalized linear mixed effects models.Expected Outcomes & Relationship to Program Area Priorities: Do current dietary approaches over supply iron resulting in inflammation and fueling pathogen growth? Does withholding iron induce metabolic stress in S. enterica and lead to unintended increases in virulence genes? Does iron bioavailability significantly reduce S. enterica load in pre- and post-harvest poultry? By addressing these questions, this basic research project will help improve animal health, nutrition, and food safety, and the ability of the US industry to produce high quality poultry products more profitably and sustainably. By testing the novel applications of an existing, FDA-approved functional feed supplements, this proposed study will advance efforts to develop more integrated, nutrition-based interventions to combatting food-borne infections as well as antimicrobial resistance. By developing theory to improve our understanding of disease transmission and pathogen evolution, this proposal addresses multiple NSF goals and NIFA foundation priority Food Safety and Defense to promote research that sustains the competitiveness and long-term sustainability of US agriculture and fosters consumer trust. Finally, this project will improve our understanding of transmission dynamics in poultry systems, which are major culprits of pathogen spillovers to humans and the environment and also harbor and transmit genes that confer antimicrobial resistance. More broadly, this project will improve our understanding of the ecological and evolutionary factors that govern disease transmission, which is critical for managing disease outbreaks and for predicting and responding to future disease emergence and spillovers from livestock and wildlife to humans.

Progress 05/01/23 to 04/30/24

Outputs
Target Audience:The target audience for this research includes poultry farmers and extension agents interested in strategies to sustainably increase the health of poultryalso reducing the potential for food-borne illnesses, especially atpre-harvest stages. These stakeholders will benefit from the identification of alternative control methods and integrated control systems for animal diseases. Additionally, this project will address significant knowledge gaps surrounding how nutritional interventions alter the retention and transmission of pathogens and genes conferring AMR. Changes/Problems:For Aim 2, conversations with stakeholders revealed concerns over any potential interactions of SQM with the vaccine for Salmonella, which is increasingly common in the poultry industry. Therefore, our first round of experiments included a fully factorial design: +/- Vaccine x +/- Salmonella enterica x +/- SQM. Our preliminary results indicate the SQM does not interact with or disrupt the efficacy of the vaccine. We are currently analyzing the 16S data from these assays. Final results from these analyses will inform the next steps. Given outbreaks due to avain influenze in both 2023 and 2024, conducting in vivo assays with poultry has proven exceptionally challenging. Moreover, the limited funds made it virtually impossible to hire a postdoctoral fellow with the training required to carry out the proposed experiments; To be competitive in the current market, postdocs are being offer three years of funding. Therefore, we are looking for alternative avenues to purse relevant questions related to pre-harvest control of Salmonella in poultry that meet these logistical and budgetary constraints. What opportunities for training and professional development has the project provided?This project has provided opportunities for the PIs Dr. Hite and Dr. Ricke and their trainees, two PhD Students (Jessica Brown and Eldon Ager) and a Postdoctoral fellow, to present seminars on preliminary findings at scientific and industry conferences. In addition, an undergraduate student, Jonny Compton is gaining invaluable research experience as a research assistant helping with DNA extraction for this project. How have the results been disseminated to communities of interest?Results from year 1 have been presented at industry and scientificseminars. What do you plan to do during the next reporting period to accomplish the goals?The next phase of the project will involve the completion of next-generation sequencing for the remaining tissue samples followed by statistical analyses, and publication.

Impacts
What was accomplished under these goals? In the first year of the grant funding period, the PI Jessica Hite worked with the co-PI Dr. Steven Ricke, a PhD student Jessica Brown, and a postdoctoral researcher Colette Nickodem to conduct and analyses the in vitro assays (Aim 1) and the first round of in vivo infection assays (Aim 2). For Aim 2, conversations with stakeholders revealed concerns over any potential interactions of SQM with the vaccine for Salmonella, which is increasingly common in the poultry industry. Therefore, our first round of experiments included a fully factorial design: +/- Vaccine x +/- Salmonella enterica x +/- SQM. Our preliminary results indicate the SQM does not interact with or disrupt the efficacy of the vaccine. In Year 2, we will repeat this experiment in Block 2 (to obtain sufficient sample sizes based on power analyses). A key goal of this proposal is to examine the potential for SQM to alter the overall microbiome and the evolutionary selective pressures that together, drive key changes in virulence (harm to host) and/or drug resistance. To address these questions, Dr. Hite, Jessica Brown, and Dr. Nickodem are working with the Research Technician, Dr. Eric Neeno-Eckwall and key collaborator, Dr. Rothrock to apply 16S and shotgun metagenomics analyses from the in vivo experiments. Dr. Rothrock provided assistance with identifying the key plasmids to focus on for the inital analyses. Preliminary 16S analysis suggests that SQM shifts the overall abundance and diversity of the gut microbiome. Dr. Nickodem is currently analyzing the shotgun metagenomic data.

Publications